Colour Morphs as Alternative Solutions to the Trade-Off Predicted by the Immuno-Competence Handicap Hypothesis

Abstract

Colour morphs in polymorphic species are associated with a suite of heritable traits governed by distinct genetic loci, each corresponding to alternative fitness peaks. Hormonal pleiotropy has been proposed as a mechanism maintaining these morphs, though experimental evidence is lacking. In this study, we tested whether white and yellow morphs of the common wall lizard (Podarcis muralis) adopt alternative strategies shaped by the immuno-competence handicap hypotheses (ICHH). Specifically, we experimentally elevated plasma testosterone levels via transdermal administration and measured changes in (i) immune response using phytohaemagglutinin (PHA) swelling and (ii) the aggressive behaviour in response to a mirror test simulating territorial intrusion. We found that testosterone-induced immune suppression was stronger in white males, while aggression decreased in both morphs. Elevated testosterone eliminated the baseline differences between morphs in both immunity and aggression. These findings provide the first experimental support for morph-specific life-history strategies in common wall lizards, consistent with the ICHH: Yellow males prioritize aggression over immunity, while white males invest more in survival at the cost of competitiveness.

Keywords

aggressive behaviour / colour morphs / immune-competence / polymorphism / trade-off

References

[1] Altunışık, A., T. E. Kalayci, İ. Uysal, M. Tosunoğlu, and N. Özdemir. 2016. “Age, Adult Survival Rate, and Adult Life Expectancy of a Podarcis tauricus Population (Reptilia: Lacertidae) from Saros Bay, Turkey.” Russian Journal of Herpetology 23: 278–282.

[2] Andrade, P., C. Pinho, G. P. I. de Lanuza, et al. 2019. “Regulatory Changes in Pterin and Carotenoid Genes Underlie Balanced Color Polymorphisms in the Wall Lizard.” Proceedings of the National Academy of Sciences of the United States of America 116: 5633–5642.

[3] Auer, K. E., M. Kußmaul, E. Möstl, K. Hohlbaum, T. Rülicke, and R. Palme. 2020. “Measurement of Fecal Testosterone Metabolites in Mice: Replacement of Invasive Techniques.” Animals 10: 165.

[4] Baeckens, S., K. Huyghe, R. Palme, and R. Van Damme. 2016. “Chemical Communication in the Lacertid Lizard Podarcis muralis: The Functional Significance of Testosterone.” Acta Zoologica 98: 94–103.

[5] Baeckens, S., and R. Van Damme. 2018. “Immunocompetence and Parasite Infestation in a Melanistic and Normally-Coloured Population of the Lacertid Lizard, Podarcis siculus.” Amphibia-Reptilia 39: 471–478.

[6] Barbault, R., and Y.-P. Mou. 1988. “Population Dynamics of the Common Wall Lizard, Podarcis muralis, in Southwestern France.” Herpetologica 44: 38–47.

[7] Barron, D. G., M. S. Webster, and H. Schwabl. 2015. “Do Androgens Link Morphology and Behaviour to Produce Phenotype-Specific Behavioural Strategies?” Animal Behaviour 100: 116–124.

[8] Belliure, J., L. C. Smith, and G. Sorci. 2004. “Effect of Testosterone on T Cell-Mediated Immunity in Two Species of Mediterranean Lacertid Lizards.” Journal of Experimental Zoology 301A: 411–418.

[9] Biaggini, M., P. Bombi, M. Capula, and C. Corti. 2011. “Podarcis muralis (Laurenti, 1768).” In Fauna D'Italia, edited by C. Corti, M. Capula, L. Luiselli, and E. Razzetti, 391–401. Calderini.

[10] Bickel, D. R., and R. Frühwirth. 2006. “On a Fast, Robust Estimator of the Mode: Comparisons to Other Robust Estimators with Applications.” Computational Statistics and Data Analysis 50: 3500–3530.

[11] Braña, F., F. Gonzalez, and A. Barahora. 1992. “Relationship Between Ovarian and Fat Body Weights During Vitellogenesis for Three Species of Lacertid Lizards.” Journal of Herpetology 26: 515–518.

[12] Calsbeek, B., D. Hasselquist, and J. Clobert. 2010. “Multivariate Phenotypes and the Potential for Alternative Phenotypic Optima in Wall Lizard (Podarcis muralis) Ventral Colour Morphs.” Journal of Evolutionary Biology 23: 1138–1147.

[13] Castilla, A. M., and D. Bauwens. 2000a. “Reproductive Characteristics of the Lacertid Lizard Podarcis atrata.” Copeia 2000: 748–756.

[14] Castilla, A. M., and D. Bauwens. 2000b. “Reproductive Characteristics of the Lacertid Island Lacertid Lizard Podarcis lilfordi.” Journal of Herpetology 34: 390–396.

[15] Chondropoulos, B. P., and J. J. Lykakis. 1983. “Ecology of the Balkan Wall Lizard, Podarcis taurica ionica (Sauria: Lacertidae) from Greece.” Copeia 1983: 991.

[16] Coladonato, A. J., M. Mangiacotti, S. Scali, et al. 2020. “Morph-Specific Seasonal Variation of Aggressive Behaviour in a Polymorphic Lizard Species.” PeerJ 8: e10268.

[17] Comendant, T., B. R. Sinervo, E. I. Svensson, and J. C. Wingfield. 2003. “Social Competition, Corticosterone and Survival in Female Lizard Morphs.” Journal of Evolutionary Biology 16: 948–955.

[18] Cox, R. M., and H. B. John-Alder. 2007. “Increased Mite Parasitism as a Cost of Testosterone in Male Striped Plateau Lizards Sceloporus virgatus.” Functional Ecology 21: 327–334.

[19] DeNardo, D. F., and B. R. Sinervo. 1994. “Effects of Steroid Hormone Interaction on Activity and Home-Range Size of Male Lizards.” Hormones and Behavior 28: 273–287.

[20] Dijkstra, P. D., O. Seehausen, M. E. R. Pierotti, and T. G. G. Groothuis. 2007. “Male-Male Competition and Speciation: Aggression Bias Towards Differently Coloured Rivals Varies Between Stages of Speciation in a Lake Victoria Cichlid Species Complex.” Journal of Evolutionary Biology 20: 496–502.

[21] Ficetola, G. F., I. Silva-Rocha, M. A. Carretero, et al. 2021. “Status of the Largest Extant Population of the Critically Endangered Aeolian Lizard Podarcis raffonei (Capo Grosso, Vulcano island).” PLoS ONE 16: e0253361.

[22] Folstad, I., and A. J. Karter. 1992. “Parasites, Bright Males, and the Immunocompetence Handicap.” American Naturalist 139: 603–622.

[23] Ford, E. B. 1945. “Polymorphisms.” Heredity 20: 73–88.

[24] Friard, O., and M. Gamba. 2016. “BORIS: A Free, Versatile Open-Source Event-Logging Software for Video/Audio Coding and Live Observations.” Methods in Ecology and Evolution 7: 1325–1330.

[25] Galán, P. 1997. “Reproductive Ecology of the Lacertid Lizard Podarcis bocagei.” Ecography 13: 197–209.

[26] Galán, P. 2004. “Structure of a Population of the Lizard Podarcis bocagei in Northwest Spain: Variations in Age Distribution, Size Distribution and Sex Ratio.” Animal Biology 54: 57–75.

[27] Galeotti, P., R. Sacchi, D. Pellitteri-Rosa, et al. 2013. “Colour Polymorphism and Alternative Breeding Strategies: Effects of Parent's Colour Morph on Fitness Traits in the Common Wall Lizard.” Evolutionary Biology 40: 385–394.

[28] Horton, B. M., M. E. Hauber, and D. L. Maney. 2012. “Morph Matters: Aggression Bias in a Polymorphic Sparrow.” PLoS ONE 7: e48705.

[29] Hover, E. L. 1985. “Differences in Aggressive Behavior Between Two Throat Color Morphs in a Lizard, Urosaurus ornatus.” Copeia 1985: 933–940.

[30] Huxley, J. S. 1955. “Morphism in Birds.” In Acta 6th International Ornithological Congress, Basel, 309–328.

[31] Klukowski, M., and C. E. Nelson. 2001. “Ectoparasite Loads in Free-Ranging Northern Fence Lizards, Sceloporus undulatus hyacinthinus: Effects of Testosterone and Sex.” Behavioral Ecology and Sociobiology 49: 289–295.

[32] Knapp, R., and M. C. Moore. 1997. “Male Morphs in Tree Lizards Have Different Testosterone Responses to Elevated Levels of Corticosterone.” General and Comparative Endocrinology 107: 273–279.

[33] Kruschke, J. K. 2010. “Bayesian Data Analysis.” Wiley Interdisciplinary Reviews: Cognitive Science 1: 658–676.

[34] Kurtz, J., M. Kalbe, Å. Langefors, I. Mayer, M. Milinski, and D. Hasselquist. 2007. “An Experimental Test of the Immunocompetence Handicap Hypothesis in a Teleost Fish: 11-Ketotestosterone Suppresses Innate Immunity in Three-Spined Sticklebacks.” American Naturalist 170: 509–519.

[35] MacLean, G. S., A. K. Lee, and K. J. Wilson. 1973. “A Simple Method of Obtaining Blood from Lizards.” Copeia 1973: 338–339.

[36] Mangiacotti, M., M. Fumagalli, M. Cagnone, et al. 2019. “Morph-Specific Protein Patterns in the Femoral Gland Secretions of a Colour Polymorphic Lizard.” Scientific Reports 9: 8412.

[37] Marler, C. A., and M. C. Moore. 1988. “Evolutionary Costs of Aggression Revealed by Testosterone Manipulations in Free-Living Male Lizards.” Behavioral Ecology and Sociobiology 23: 21–26.

[38] Marler, C. A., and M. C. Moore. 1989. “Time and Energy Costs of Aggression in Testosterone-Implanted Free Living Male Mountain Spiny Lizards Sceloporus jarrovi.” Physiological Zoology 62: 1334–1350.

[39] McKinnon, J. S., and M. E. R. Pierotti. 2010. “Colour Polymorphism and Correlated Characters: Genetic Mechanisms and Evolution.” Molecular Ecology 19: 5101–5125.

[40] Meredith, M., and J. K. Kruschke. 2018. HDInterval: Highest (Posterior) Density Intervals (R package version 0.2.0). https://CRAN.R-project.org/package=HDInterval.

[41] Munck, A., P. M. Guyre, and N. J. Holbrook. 1984. “Physiological Functions of Glucocorticoids in Stress and Their Relation to Pharmacological Actions.” Endocrine Reviews 5: 25–44.

[42] Olsson, M., E. Wapstra, T. Madsen, and B. Silverin. 2000. “Testosterone, Ticks and Travels: A Test of the Immunocompetence-Handicap Hypothesis in Free-Ranging Male Sand Lizards.” Proceedings of the Royal Society B: Biological Sciences 267: 2339–2343.

[43] Oppliger, A., M. S. Giorgi, A. Conelli, M. Nembrini, and H. B. John-Alder. 2004. “Effect of Testosterone on Immunocompetence, Parasite Load, and Metabolism in the Common Wall Lizard (Podarcis muralis).” Canadian Journal of Zoology 82: 1713–1719.

[44] Palme, R. 2005. “Measuring Fecal Steroids: Guidelines for Practical Application.” Annals of the New York Academy of Sciences 1046: 75–80.

[45] Palme, R., C. Touma, N. Arias, M. F. Dominchin, and M. Lepschy. 2013. “Steroid Extraction: Get the Best out of Faecal Samples.” Wiener Tierarztliche Monatsschrift 100: 238–246.

[46] Pérez i de Lanuza, G., E. Font, and P. Carazo. 2013. “Color-Assortative Mating in a Color-Polymorphic Lacertid Lizard.” Behavioral Ecology 24: 273–279.

[47] Poncet, P. 2012. modeest: Mode Estimation. http://cran.r-project.org/package=modeest.

[48] R Core Team. 2022. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.r-project.org/.

[49] Sacchi, R., A. J. Coladonato, M. Battaiola, et al. 2021. “Subjective Resource Value Affects Aggressive Behavior Independently of Resource-Holding-Potential and Color Morphs in Male Common Wall Lizard.” Journal of Ethology 39: 179–189.

[50] Sacchi, R., M. Ghitti, S. Scali, et al. 2015. “Common Wall Lizard Females (Podarcis muralis) Do Not Actively Choose Males Based on Their Colour Morph.” Ethologist 121: 1145–1153.

[51] Sacchi, R., M. Mangiacotti, S. Scali, M. Ghitti, and M. A. L. Zuffi. 2017a. “Effects of Colour Morph and Temperature on Immunity in Males and Females of the Common Wall Lizard.” Evolutionary Biology 44: 496–504.

[52] Sacchi, R., D. Pellitteri-Rosa, A. Bellati, et al. 2013. “Colour Variation in the Polymorphic Common Wall Lizard (Podarcis muralis): An Analysis Using the RGB Colour System.” Zoologischer Anzeiger 252: 431–439.

[53] Sacchi, R., D. Pellitteri-Rosa, A. Capelli, et al. 2012. “Studying the Reproductive Biology of the Common Wall Lizard Using Ultrasonography.” Journal of Zoology 287: 301–310.

[54] Sacchi, R., F. Pupin, A. Gentilli, et al. 2009. “Male-Male Combats in a Polymorphic Lizard: Residency and Size, but Not Color, Affect Fighting Rules and Contest Outcome.” Aggressive Behavior 35: 274–283.

[55] Sacchi, R., D. Rubolini, A. Gentilli, et al. 2007a. “Morph-Specific Immunity in Male Podarcis muralis.” Amphibia-Reptilia 28: 408–412.

[56] Sacchi, R., S. Scali, M. Mangiacotti, et al. 2017b. “Seasonal Variations of Plasma Testosterone Among Colour-Morph Common Wall Lizards (Podarcis muralis).” General and Comparative Endocrinology 240: 114–120.

[57] Sacchi, R., S. Scali, F. Pupin, A. Gentilli, P. Galeotti, and M. Fasola. 2007b. “Microgeographic Variation of Colour Morph Frequency and Biometry of Common Wall Lizards.” Journal of Zoology 273: 389–396.

[58] Scali, S., M. Mangiacotti, R. Sacchi, et al. 2021. “Close Encounters of the Three Morphs: Does Color Affect Aggression in a Polymorphic Lizard?” Aggressive Behavior 47: 430–438.

[59] Scali, S., R. Sacchi, M. Azzusi, S. Daverio, T. Oppedisano, and M. Mangiacotti. 2013. “Homeward Bound: Factors Affecting Homing Ability in a Polymorphic Lizard.” Journal of Zoology 289: 196–203.

[60] Scali, S., R. Sacchi, M. Falaschi, et al. 2019. “Mirrored Images but Not Silicone Models Trigger Aggressive Responses in Male Common Wall Lizards.” Acta Herpetologica 14: 35–41.

[61] Sillero, N., J. Campos, A. Bonardi, et al. 2014. “Updated Distribution and Biogeography of Amphibians and Reptiles of Europe.” Amphibia-Reptilia 35: 1–31.

[62] Sinervo, B. R., and C. M. Lively. 1996. “The Rock-Paper-Scissors Game and the Evolution of Alternative Male Strategies.” Nature 380: 240–243.

[63] Sinervo, B. R., and E. I. Svensson. 2002. “Correlational Selection and the Evolution of Genomic Architecture.” Heredity 89: 329–338.

[64] Sinervo, B. R., E. I. Svensson, and T. Comendant. 2000. “Density Cycles and an Offspring Quantity and Quality Game Driven by Natural Selection.” Nature 406: 985–988.

[65] Su, U., and M. Yajima. 2015. R2jags: Using R to Run “JAGS.” (R package version 0.5-7). http://cran.r-project.org/package=R2jags.

[66] Svensson, E. I. 2017. “Back to Basics: Using Colour Polymorphisms to Study Evolutionary Processes.” Molecular Ecology 26: 2204–2211.

[67] Svensson, E. I., B. R. Sinervo, and T. Comendant. 2001. “Condition, Genotype-by-Environment Interaction, and Correlational Selection in Lizard Life-History Morphs.” Evolution; International Journal of Organic Evolution 55: 2053–2069.

[68] Whitlock, M. C., P. C. Phillips, F. B. G. Moore, and S. J. Tonsor. 1995. “Multiple Fitness Peaks and Epistasis.” Annual Review of Ecology and Systematics 26: 601–629.

[69] Yewers, M. S. C., S. R. Pryke, and D. Stuart-Fox. 2016. “Behavioural Differences Across Contexts May Indicate Morph-Specific Strategies in the Lizard Ctenophorus decresii.” Animal Behaviour 111: 329–339.

RIGHTS & PERMISSIONS

2025 The Author(s). Integrative Zoology published by International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.